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Title: Characterization of foodborne Staphylococcus aureus isolates: association of toxin gene profile with genotype and food commodities in Shanghai, China

Author
item SONG, MINGHUI - Shanghai Jiaotong University
item YALONG, BAI - Shanghai Jiaotong University
item JIE, XU - Shanghai Jiaotong University
item Carter, Michelle
item CHUNLEI, SHI - Shanghai Jiaotong University
item SHI, XAINMING - Shanghai Jiaotong University

Submitted to: International Journal of Food Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/22/2014
Publication Date: 11/29/2014
Citation: Song, M., Yalong, B., Jie, X., Carter, M.Q., Chunlei, S., Shi, X. 2014. Characterization of foodborne Staphylococcus aureus isolates: association of toxin gene profile with genotype and food commodities in Shanghai, China. International Journal of Food Microbiology. doi: 10.1016/j.ijfoodmicro.2014.11.020.

Interpretive Summary: The bacterial pathogen Staphylococcus aureus is often found in food. In this study, we compared the common and different features of S. aureus food isolates with strains that are known to cause severe human infections. A total of 142 Staphylococcus aureus strains were isolated from five different commercial foods in Shanghai, China. First, we found that these food isolates differed largely in their genetic makeup (genotype). Using different strain classification methods, we categorized these 142 strains to 16 MLST Clone Complexes (CCs), 34 spa types, and 6 agr groups. We then examined the presence of genes encoding S. aureus toxins and found that about 72.5% of S. aureus isolates were positive for at least one toxin gene. Thus, those isolates were considered as toxigenic strains. We further investigated if a particular food was associated with a particular toxigenic strain and discovered that high percentages of milk and meat isolates were carrying toxin genes. Additionally, S. aureus isolates from milk, meat and bean products contained more toxin genes (toxin gene content) and exhibited greater toxin gene diversity than those from frozen foods or fresh vegetables/fruits. Taking together, our data suggest that, in addition to milk and meat, bean products also served as a potential source of highly toxigenic S. aureus.

Technical Abstract: Staphylococcus aureus is an important clinical and foodborne pathogen. Zoonotic risk of transmission to humans highlights the need to understand the ecology of S. aureus in various foods. We characterized the genetic diversity and the distribution of 25 toxin genes in 142 foodborne Staphylococcus aureus isolates. The genotypes were determined by MLST, spa and agr typing; toxin genes were detected by PCR and verified by sequencing. The S. aureus isolates were grouped in 16 MLST Clone Complexes (CCs), 34 spa types, and 6 agr groups. CC188-t189-' was the dominant and the only common genotype among S. aureus isolates from various foods. 72.5% of S. aureus isolates were positive for at least one targeted toxin gene, thus were considered as toxigenic strains. A high percentage of toxigenic strains were found in both milk (89.7%) and meat (80.0%) isolates. S. aureus isolates from milk, meat and bean products carried more toxin genes and exhibited greater diversity of toxin genes than those from frozen foods or fresh vegetables/fruits. The average number of toxin genes for CC5, CC9, CC20, CC50, and CC72 was above 5, significantly higher than any other CCs, indicating a link of highly toxigenic strains to certain genotypes. Distinct toxin gene profiles were observed for strains with identical genotypes, suggesting a role of horizontal gene transfer in emergence of toxigenic S. aureus strains. Our study revealed that, in addition to milk and meat, bean products also served as an important source of highly toxigenic S. aureus.